The intrinsic dynamics of retinal bipolar cells isolated from tiger salamander

We studied how intrinsic membrane properties affect the gain and temporal pattern of response in bipolar cells dissociated from retinae of tiger salamanders. Currents specified by a pseudorandom binary sequence, an m-sequence, superimposed on various means, were injected into the cells. From the resultant membrane voltage response for each mean current, impulse responses were estimated. From each impulse response, transfer function, gain, and time constant were calculated. The bipolar cells acted as quasilinear adaptive filters whose gain and response speed are determined by the mean input current. Near resting potential, gain, and time constant were maximum. Dynamics were slow and low-pass, characterized by an approximately exponential impulse response. With depolarization, gains were reduced sharply, responses were much faster, and dynamics became band-pass, as indicated by an undershoot in the impulse response. For any given mean current, the shape of the impulse response did not depend on the amplitude of the m-sequence currents. Thus, bipolar cells behaved in a quasilinear fashion. The adaptive behavior was eliminated by blocking a potassium current, which implicates the role of a voltage-gated potassium conductance. Computer simulations on a model neuron including a delayed-rectifier reconstructed the observed behavior, and provided insight into other, less readily observable, parameters. Thus, bipolar cells, even when isolated, possess mechanisms which regulate, with unsuspected elaborateness, the sensitivities and dynamics of their responsiveness. Implications for adaptation and neuronal processing are discussed.

[1]  M. Slaughter,et al.  Functional properties of a metabotropic glutamate receptor at dendritic synapses of ON bipolar cells in the amphibian retina , 1995, Visual Neuroscience.

[2]  S. Ito,et al.  The Shaker-like potassium channels of the mouse rod bipolar cell and their contributions to the membrane current , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  R. Miller,et al.  Properties of synaptic transmission from photoreceptors to bipolar cells in the mudpuppy retina. , 1993, Journal of neurophysiology.

[4]  S. Wu,et al.  Modulation of synaptic gain by light. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[5]  A. Lasansky,et al.  Properties of depolarizing bipolar cell responses to central illumination in salamander retinal slices , 1992, Brain Research.

[6]  G. Falk,et al.  Properties of the cGMP-activated channel of retinal on-bipolar cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  William H. Press,et al.  Numerical Recipes in C, 2nd Edition , 1992 .

[8]  P. MacLeish,et al.  Glutamate and 2-amino-4-phosphonobutyrate evoke an increase in potassium conductance in retinal bipolar cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[9]  S. Wu Chapter 2 Signal transmission and adaptation-induced modulation of photoreceptor synapses in the retina , 1991 .

[10]  Scott Nawy,et al.  Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells , 1990, Nature.

[11]  H. Wässle,et al.  Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. , 1990, Journal of neurophysiology.

[12]  R. Shapley,et al.  Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells , 1990, Visual Neuroscience.

[13]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990, Bulletin of mathematical biology.

[14]  J. Victor The dynamics of the cat retinal Y cell subunit. , 1988, The Journal of physiology.

[15]  E M Lasater,et al.  Membrane currents of retinal bipolar cells in culture. , 1988, Journal of neurophysiology.

[16]  K. Yau,et al.  Calcium and light adaptation in retinal rods and cones , 1988, Nature.

[17]  B. Rudy,et al.  Diversity and ubiquity of K channels , 1988, Neuroscience.

[18]  D. Copenhagen,et al.  Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). , 1988, The Journal of physiology.

[19]  P Mobbs,et al.  Membrane Currents in Retinal Bipolar Cells of the Axolotl , 2003 .

[20]  G. Falk Signal transmission from rods to bipolar and horizontal cells: A synthesis , 1988 .

[21]  W. G. Owen,et al.  Voltage gain of signal transfer from retinal rods to bipolar cells in the tiger salamander. , 1987, The Journal of physiology.

[22]  Martin Wilson,et al.  Signal clipping by the rod output synapse , 1987, Nature.

[23]  D. Attwell,et al.  The Sharpey-Schafer lecture. Ion channels and signal processing in the outer retina. , 1986, Quarterly journal of experimental physiology.

[24]  G Owen,et al.  Morphology of physiologically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum , 1986, The Journal of comparative neurology.

[25]  A. Kaneko,et al.  Chapter 5 Membrane properties of solitary retinal cells , 1986 .

[26]  A. Kaneko,et al.  A voltage‐clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. , 1985, The Journal of physiology.

[27]  J. Dowling,et al.  Pharmacological properties of isolated horizontal and bipolar cells from the skate retina , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  E. A. Schwartz,et al.  Control of the generator current in solitary rods of the Ambystoma tigrinum retina. , 1984, The Journal of physiology.

[29]  D. Tranchina,et al.  Retinal light adaptation—evidence for a feedback mechanism , 1984, Nature.

[30]  J. Ashmore,et al.  Kinetics of synaptic transmission from photoreceptors to horizontal and bipolar cells in turtle retina , 1983, Vision Research.

[31]  C. Barnstable,et al.  Use of a monoclonal antibody as a substrate for mature neurons in vitro. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Edward H. Adelson,et al.  Saturation and adaptation in the rod system , 1982, Vision Research.

[33]  D. Cole Adler's Physiology of the Eye: Clinical Application , 1982 .

[34]  D Bertrand,et al.  Voltage‐activated and calcium‐activated currents studied in solitary rod inner segments from the salamander retina , 1982, The Journal of physiology.

[35]  S. Naghshineh,et al.  Action of glutamate and aspartate analogues on rod horizontal and bipolar cells , 1981, Nature.

[36]  A. Kaneko,et al.  Retinal bipolar cells with double colour-opponent receptive fields , 1981, Nature.

[37]  M. Slaughter,et al.  2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. , 1981, Science.

[38]  J. Ashmore,et al.  Different postsynaptic events in two types of retinal bipolar cell , 1980, Nature.

[39]  G Falk,et al.  Responses of rod‐bipolar cells in the dark‐adapted retina of the dogfish, Scyliorhinus canicula , 1980, The Journal of physiology.

[40]  J. Ashmore,et al.  Transmission of visual signals to bipolar cells near absolute threshold , 1979, Vision Research.

[41]  K. Naka,et al.  Morphological and functional identifications of catfish retinal neurons. II. Morphological identification. , 1975, Journal of neurophysiology.

[42]  K. Naka,et al.  Morphological and functional identifications of catfish retinal neurons. III. Functional identification. , 1975, Journal of neurophysiology.

[43]  A. Hodgkin,et al.  Changes in time scale and sensitivity in turtle photoreceptors , 1974, The Journal of physiology.

[44]  C. Enroth-Cugell,et al.  Adaptation and dynamics of cat retinal ganglion cells , 1973, The Journal of physiology.

[45]  D. H. Kelly Adaptation effects on spatio-temporal sine-wave thresholds. , 1972, Vision research.

[46]  F. Werblin Adaptation in a vertebrate retina: intracellular recording in Necturus. , 1971, Journal of neurophysiology.

[47]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[48]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.